Nutrition usually makes a small but potentially valuable contribution to successful performance in elite athletes, and dietary supplements can make a minor contribution to this nutrition program. Nonetheless, supplement use is widespread at all levels of sport. Products described as supplements target different issues, including the management of micronutrient deficiencies, supply of convenient forms of energy and macronutrients, and provision of direct benefits to performance or indirect benefits such as supporting intense training regimens. The appropriate use of some supplements can offer benefits to the athlete, but others may be harmful to the athlete’s health, performance, and/or livelihood and reputation if an anti-doping rule violation results. A complete nutritional assessment should be undertaken before decisions regarding supplement use are made. Supplements claiming to directly or indirectly enhance performance are typically the largest group of products marketed to athletes, but only a few (including caffeine, creatine, specific buffering agents and nitrate) have good evidence of benefits. However, responses are affected by the scenario of use and may vary widely between individuals because of factors that include genetics, the microbiome, and habitual diet. Supplements intended to enhance performance should be thoroughly trialed in training or simulated competition before implementation in competition. Inadvertent ingestion of substances prohibited under the anti-doping codes that govern elite sport is a known risk of taking some supplements. Protection of the athlete’s health and awareness of the potential for harm must be paramount, and expert professional opinion and assistance is strongly advised before embarking on supplement use.

Dietary supplements are used by athletes at all levels of sport, reflecting the prevalence of their use in the wider society. About half of the adult US population uses some form of dietary supplements (Bailey et al., 2011) and, though there are regional, cultural, and economic differences, a similar prevalence is likely in many other countries. Athletes describe a range of different reasons for their supplement choices (Fennell, 2004), and products that fit the description of “supplement” can target various roles within the athlete’s performance plan. These include the maintenance of good health by contributing to the required intake of specific nutrients, the management of micronutrient deficiencies, and the provision of energy and macronutrient needs that might be difficult to achieve through food intake alone. Other specific uses of supplements reported by athletes include direct performance enhancement or the indirect benefits that arise from the provision of support for hard training, the manipulation of physique, the alleviation of musculoskeletal pain, rapid recovery from injury, and enhancement of mood.

Some sporting bodies now support the pragmatic use of supplements that have passed a risk-vs.-benefit analysis of being effective, safe, and permitted for use, while also being appropriate to the athlete’s age and maturation in their sport. This review summarizes the issues faced by high-performance athletes and their support team (coach, trainer, nutritionist, physician) when considering the use of supplements, with the goal of providing information to assist them to make informed decisions.

What is a Supplement?

There is no single definition, either legal or within nutritional science, of what constitutes a dietary supplement. The US Congress, for example, in framing the 1994 Dietary Supplements Health and Education Act (DSHEA), described a dietary supplement as: “. . . a product, other than tobacco, which is used in conjunction with a healthy diet and contains one or more of the following dietary ingredients: a vitamin, mineral, herb or other botanical, an amino acid, a dietary substance for use by man to supplement the diet by increasing the total daily intake, or a concentrate, metabolite, constituent, extract, or combinations of these ingredients” (Office of Dietary Supplements, National Institutes of Health, 1994).

This definition is unsatisfactory, as it depends on whether or not a “healthy diet” is consumed. For the purposes of this overview, we define a dietary supplement as: A food, food component, nutrient, or nonfood compound that is purposefully ingested in addition to the habitually-consumed diet with the aim of achieving a specific health and/or performance benefit.

Furthermore, we recognize that dietary supplements come in many forms, including:

(a)Functional foods: foods enriched with additional nutrients or components outside their typical nutrient composition (e.g., mineral- and vitamin-fortified, as well as nutrient-enriched foods)

(b)Formulated foods and sports foods: products providing energy and nutrients in a more convenient form than normal foods for general nutrition support (e.g., liquid meal replacements) or for targeted use around exercise (e.g., sports drinks, gels, bars)

(c)Single nutrients and other components of foods or herbal products provided in isolated or concentrated forms

(d)Multi-ingredient products containing various combinations of those products described above that target similar outcomes

Prevalence of, and Rationale for, Use by Athletes

With such widespread use of supplements in the general population and with the specific focus of athletes on achieving peak performance, it is not surprising that a high prevalence of supplement use is reported in most surveys of athletes (Maughan et al., 2007). Comparisons between surveys are confounded by numerous factors. These include differences in the definition of what constitutes a dietary supplement; ability to capture irregular use; inappropriate sample selection; and the use of nonvalidated and nonstandardized survey instruments (Garthe & Maughan, 2018). Nevertheless, surveys generally suggest that supplement use:

Although athletes often consume supplements to take advantage of intended/claimed effects or benefits, a range of motives underpins supplement use (Garthe & Maughan, 2018). For example, athletes use supplements:

(a)To correct or prevent nutrient deficiencies that may impair health or performance

(b)For convenient provision of energy and nutrients around an exercise session

(c)To achieve a specific and direct performance benefit in competition

(e)For financial gain (sponsorship) or because products are provided free of charge

(f)As a “just in case” insurance policy

(g)Because they know or believe that other athletes/competitors are using the supplement(s)

Some supplements may be used for multiple functions. Zinc, for example, may be taken with the aim of promoting wound healing and tissue repair (Prasad, 2014) or reducing the severity and duration of the symptoms of an upper respiratory tract infection (Solomons, 1998). Carbohydrate supplements are used to enhance performance in many events via the provision of fuel substrate (Stellingwerff & Cox, 2014), to support the immune system (Peake et al., 2017), or to improve bioavailability of other supplements (e.g., creatine; Steenge et al., 2000). Similarly, creatine supplementation may directly enhance performance in strength and power events, and can assist in training harder, gaining lean body mass, or maintaining lean mass during periods of immobilization after injury (Branch, 2003; Gualano et al., 2012; Heaton et al., 2017). Decisions on supplement use therefore need to consider both the context of use and the specific protocol employed.

Assessing the Evidence Base for Supplement Use

Supplements target a range of scenarios of use, so different approaches are needed to assess their effectiveness. Supplements aimed at correcting nutrient deficiencies need to be judged on their ability to prevent or treat suboptimal nutrient status, with the benefit accruing from the removal of the associated impairment of health, training capacity, or performance. The effectiveness of sports foods might be hard to isolate when they are used within the general diet to meet everyday energy needs and nutrient targets. However, benefits may be more easily detected when they are specifically consumed before, during, or after an event or training session to provide nutrients that are limiting for performance (e.g., to provide fuel for the muscle or brain) or to defend homeostasis (e.g., by replacing water and salt losses). Performance-enhancing supplements which are claimed to achieve direct or indirect benefits pose a greater challenge in terms of a sound evidence base. With only a few exceptions, there is a scarcity of research, and many of the available studies are not of sufficient quality to warrant their application to elite athletes.

Substantiating the claims made about performance supplements and sports foods is difficult (Burke & Peeling, 2018). To various audiences, “proof” comes in different forms. Figure 1 provides a proposed hierarchical model of the relative strength of the evidence provided by different information sources. However, most of the information around supplement efficacy in sport comes from models with the lowest rigor: anecdotes/observations from athletes and scientific or mechanistic hypotheses that explain how a supplement might target a critical/limiting factor in performance, but with little to no evidence. Systematic reviews and meta-analyses, which synthesize the outputs of many studies to yield a conclusive statement of efficacy in a broad sense, are at the top of the evidence hierarchy. While these summaries help to provide information about the general use of performance supplements, scientific trials that are properly controlled and well-conducted provide the basis for these reviews, as well as an opportunity to address more specific questions about supplement applications. Thus, meta-analyses are a reflection only of the quality and quantity of the studies that are available for review, and may also be influenced by the inclusion and exclusion criteria applied to the available data.

The gold standard for investigating the effects of supplements on sports performance is the prospective, randomized, controlled scientific trial, in which subjects are randomly allocated to receive either an experimental or placebo treatment (ideally in a double-blind manner) or crossed over to receive both treatments in counterbalanced order, under standardized conditions. Practical issues may cause some variations to ideal design, but sports scientists are encouraged, if they wish their results to be applicable to athletes in competition, to ensure that their studies include:

(a)An adequate sample size and appropriate participant characteristics (e.g., event, training status, caliber) to allow the results to have statistical power and to be applicable to high-performance athletes

(c)Standardization, to the extent that is possible, of variables that might influence the results (e.g., pretrial exercise and diet, environmental conditions, external encouragement or distraction). It is recognized that this conflicts to some extent with (b) above, and will limit the situations in which the results can be applied.

(d)Use of a protocol of supplement use (e.g., specific product, dose, and timing of intake) that is likely to optimize any effects

(e)An independent verification of the contents of the supplement under investigation to ensure that the product is truly unadulterated, both to ensure the integrity of the study and to avoid inadvertent doping positives if the subjects are athletes

(f)Verification that the supplement was taken and induced a biological response (e.g., via muscle, blood, urine, or saliva sampling)

(g)A performance protocol that is valid and sufficiently reliable to detect small but potentially meaningful changes/differences in performance outcomes.

(h)Interpretation of results in light of the limitations of the study design and the change that would be meaningful to real-life sport

Given the specificity of the information that is required by some athletes and their support staff to assess the effectiveness of a supplement (e.g., related to a targeted event and its conditions, the specific individual, the combination with other performance strategies), it is unreasonable to expect that definitive evidence will always be available. Issues that are particularly under-researched and should be considered of high priority include measurement of performance in the field or under “real-life” conditions, investigation of the combined use of a number of supplements, and the repeated use of supplements as might occur in multi-day competition or when heats and finals occur close together. Scenarios that fall outside the scope of the available literature or practical research design may need to be interrogated by individual or small group case studies. Recommended methodologies for these studies include repeated baseline performances before the introduction of the supplement, or an alternating series of presentation and absence of the supplement (Burke & Peeling, 2018).

For the purposes of this overview, we rely primarily on studies of healthy adults that are relevant to athletes. We recognize that data from studies of elite athletes are almost entirely absent. We also recognize that mechanistic studies on animal and cell culture models are useful in identifying mechanisms, but a mechanism is not necessary to demonstrate an effect that may be meaningful to an athlete. What we think today to be the mechanism by which enhancement of performance or health occurs might be proved wrong by later studies. It must also be recognized that an individual’s habitual diet can affect gene expression and their microbiota, and these, in turn, can affect response to supplementation. While the variation in the genome between individuals is less than 0.01%, the variation in microbiota is significant (80–90%), and emerging data suggests that both these factors could affect athletic performance (Clark & Mach, 2017; Ribeiro et al., 2013). The following sections present an overview of the use of supplements to address different roles in sports nutrition, first by identifying the principles of use and then by examining some of the specific products that have a good or emerging evidence base to support this situation-specific use by athletes.

Supplements Used to Prevent or Treat Nutrient Deficiencies

Many micronutrients play an important role in the regulation of processes that underpin sports performance, ranging from energy production to the manufacture of new cells and proteins. A frank deficiency of one or more of these nutrients may lead to a measurable impairment of sports performance, either directly or by reducing the athlete’s ability to train effectively (e.g., iron deficiency anemia) or to stay free from illness or injury (e.g., impact of vitamin D deficiency on bone health). Athletes are not immune to the inadequate eating practices or the increased nutrient loss/requirements found in some members of the general population and may even be at greater risk of deficiencies because of increased nutrient turnover or increased losses. A further challenge is the occurrence of subclinical deficiencies that may be both hard to assess (i.e., they lack a clear metric or universal threshold of what is “adequate”) as well as subject to debate about whether there is an “optimal” level for performance that differs from the usual classification systems of nutrient status (deficiency/subclinical, deficiency/normal). When suboptimal nutritional status is diagnosed, the use of a nutrient supplement to reverse or prevent further deficiencies can contribute to the overall treatment plan.

Nutritional assessment of an athlete involves systematic protocols that obtain, verify, and interpret evidence of nutrition-related problems, as well as their causes and significance. A complete assessment should ideally include a detailed medical and nutritional history, diet evaluation, anthropometry and body composition analysis, and biochemical testing (Larson-Meyer et al., 2018). Unlike the ad hoc use of nutrient supplements taken by athletes as an insurance policy, this nutritional assessment should ensure that the athlete:

(a)Can address the factors that led to the nutrient deficiency, including ensuring that the athlete’s nutrition plan is adequate in energy, macronutrients, and micronutrients

(b)Would benefit from an acute or chronic period of supplementation to correct and/or prevent a nutrient deficiency and can understand the appropriate supplementation protocol

(c)Is not at risk for health issues associated with supplement use, including interactions with prescription or over-the-counter medications

(d)Has a baseline assessment against which future measures to assess progress can be compared

Nutrients that often need to be supplemented under these circumstances include iron, calcium, and vitamin D (Table 1). Iodine (for those living in areas with low levels of iodine in foods or not using iodized salt), folate (for women who might become pregnant), and vitamin B12 (for those following a vegan or near-vegan diet) supplementation may be warranted in these population groups, but these considerations do not apply specifically to athletes.

Table 1

Examples of Micronutrients Often Requiring Supplementation in Athletes*

No consensus over the serum 25-hydroxyvitamin D concentration (the marker of vitamin D status) that defines deficiency, insufficiency, sufficiency, and a tolerable UL; the need to supplement depends on UVB exposure and skin type

Supplementation of between 800 IU and 1,000–2,000 IU/day is recommended to maintain status for the general population. Supplementation guidelines are not yet established in athletes. Short-term, high-dose supplementation, which includes 50,000 IU/week for 8–16 weeks or 10,000 IU/day for several weeks, may be appropriate for restoring status in deficient athletes. Careful monitoring is necessary to avoid toxicity (Heaney, 2008).

Athletes who do not maintain adequate iron status may need supplemental iron at doses greater than their RDA (i.e., >18 mg/day for women and >8 mg/day for men). Athletes with iron deficiency require clinical follow-up which may include supplementation with larger doses of oral iron supplementation along with improved dietary iron intake (Thomas et al., 2016). Numerous oral iron preparations are available and most are equally effective as long as they are taken (Schrier & Auerbach, 2017). High-dose iron supplements, however, should be not taken unless iron deficiency is present.

No appropriate indicator of calcium status; bone mineral density scan may be indicative of chronic low calcium intake but other factors including suboptimal vitamin D status and disordered eating are also important

Note. Indiscriminate supplementation with any of the above nutrients is not recommended. Deficiencies should first be identified through nutritional assessment, which includes dietary intake and the appropriate blood or urinary marker, if available (Larson-Meyer et al., 2018).

Supplements (Sports Foods) Used to Provide a Practical Form of Energy and Nutrients

Sports nutrition guidelines provide clear recommendations for targeted intake of energy and nutrients in a variety of contexts. In some situations, it is impractical for an athlete to consume “everyday” or normal foods to meet their nutrition goals due to issues around preparation or storage, ease of consuming the foods due to training schedules, gut comfort, or the challenge of meeting nutrient targets within the available energy budget. In these cases, sports foods can provide a convenient, albeit usually more expensive, alternative option for meeting these nutrient goals. Table 2 provides an overview of products that fit this description and their more common evidence-based uses.

Rapid rehydration following dehydration undertaken for weight-making; replacement of large sodium losses during ultra-endurance activities; rapid postexercise rehydration following moderate to large fluid and sodium deficits

Protein supplement

Powder (mix with water or milk) or ready-to-drink liquid; protein-rich bar, usually low in CHO

Provides 20–50 g protein in a single serve from high-quality types of animal (whey, casein, milk, egg) or vegetable (e.g., soy) originNote: May contain other ingredients, some of which are not evidence based and may increase the risk of contamination

Postexercise recovery following key training sessions or events where adaptation requiring protein synthesis is desired; achievement of increase in lean mass during growth or response to resistance training; portable nutrition for busy schedule or travel

40–50 g CHO, 5–10 g protein; usually low in fat and fiber; vitamins/minerals: 50–100% of RDA/RDIsNote: May contain other ingredients, some of which are not evidence-based and may increase the risk of contamination

Supplements That Directly Improve Sports Performance

A few performance-enhancing supplements might, at the present time, be considered to have an adequate level of support to suggest that marginal performance gains may be possible. These supplements include: caffeine, creatine (in the form of creatine monohydrate), nitrate, sodium bicarbonate, and possibly also β-alanine. The mechanisms of action, typical dose, potential performance benefits, and known side-effects of each of these supplements are summarized in Table 3. Performance-enhancing supplements should be considered only where a strong evidence-base supports their use as safe, legal, and effective, and, ideally, after adequacy of sports nutrition dietary practices is ensured. Whenever possible, supplements should be trialed thoroughly by the athlete in training that mimics the competition milieu as closely as possible before committing to use in a competition setting. Athletes should do a careful risk analysis to see if the marginal gains would outweigh the risk of inadvertent doping due to contamination.

Table 3

Supplements With Good to Strong Evidence of Achieving Benefits to Performance When Used in Specific Scenarios (see Peeling et al., 2018 for further details)

Larger caffeine doses (≥9 mg/kg BM) do not appear to increase the performance benefit (Bruce et al., 2000), and are more likely to increase the risk of negative side effects, including nausea, anxiety, insomnia, and restlessness (Burke, 2008). Lower caffeine doses, variations in the timing of intake before and/or during exercise, and the need for (or lack thereof) a caffeine withdrawal period should be trialed in training prior to competition use. Caffeine consumption during activity should be considered concurrent with CHO intake for improved efficacy (Talanian & Spriet, 2016). Caffeine is a diuretic, promoting increased urine flow, but this effect is small at the doses that have been shown to enhance performance (Maughan & Griffin, 2003).

Creatine

Overview

Creatine loading can acutely enhance the performance of sports involving repeated high-intensity exercise (e.g., team sports), as well as the chronic outcomes of training programs based on these characteristics (e.g., resistance or interval training), leading to greater gains in lean mass and muscular strength and power (Rawson & Persky, 2007; Volek & Rawson, 2004).

No negative health effects are noted with long-term use (up to 4 years) when appropriate loading protocols are followed (Schilling et al., 2001). A potential 1–2 kg BM increase after creatine loading (primarily as a result of water retention; Deminice et al., 2013; Powers et al., 2003), may be detrimental for endurance performance or in events where the BM must be moved against gravity (e.g., high jump, pole vault) or where athletes must achieve a specific BM target.

The available evidence suggests there appears to be few side effects or limitations to nitrate supplementation. There may exist the potential for GI upset in susceptible athletes, and should therefore be thoroughly trialed in training. There appears to be an upper limit to the benefits of consumption (i.e., no greater benefit from 16.8 mmol [1,041 mg] vs. 8.4 mmol [521 mg]; Wylie et al., 2013). Performance gains appear harder to obtain in highly-trained athletes (Jones, 2014b).

A positive correlation between the magnitude of muscle carnosine change and performance benefit remains to be established (Saunders et al., 2016). Large interindividual variations in muscle carnosine synthesis have been reported (Nassis et al., 2016). The supplement effectiveness appears harder to realize in well-trained athletes (Bellinger, 2014). There is a need for further investigation to establish the practical use in various sport-specific situations (Hobson et al., 2012; Saunders et al., 2016). Possible negative side effects include skin rashes and/or transient paresthesia.

Supplements That Improve Performance Indirectly

Many dietary supplements claim to enhance performance indirectly by supporting the athlete’s health, body composition, and their ability to train hard, recover quickly, adapt optimally, avoid or recover from injury, and tolerate pain or soreness. Illness is a major problem for athletes if it interrupts training or occurs at a critical time, such as during a selection event or a major competition. Susceptibility to illness is increased in situations where athletes are involved in a high volume of training or competition and either intentionally or unintentionally experience deficits in energy intake (e.g., weight-loss diets), macronutrient intake (e.g. train-low or sleep-low-carbohydrate), and micronutrient status (e.g., vitamin D insufficiency in the winter) (Bermon et al., 2017). Athletes might benefit from nutritional supplements to support immunity in these scenarios and at other times when they are either susceptible to infection (e.g., during the common cold season and after long-haul travel) or suffering from an infection. Table 4 summarizes evidence for some of the commonly promoted “immune supportive” supplements, noting that the most promising candidates to assist in the prevention or treatment of upper respiratory symptoms are vitamin D and probiotics. Vitamin C during periods of heavy exertion and zinc lozenges at the onset of symptoms may be useful, but high doses of single antioxidants, particularly vitamin C and E, may blunt exercise-induced training adaptations (Nikolaidis et al., 2012; Paulsen et al., 2014; Powers et al., 2011). Probiotic supplementation may reduce the incidence of travelers’ diarrhea and gastrointestinal infection. Cochrane reviews have noted the low quality of many studies on nutritional supplements that are claimed to support immunity; specifically, small samples, poor controls, and unclear procedures for randomization and blinding were commonplace (Hao et al., 2015; Singh & Das, 2013). Clearly, there is a pressing need for randomized controlled trials in high-level athletes with sufficient participant numbers, rigorous controls and procedures, appropriate supplementation regimens, and clinically meaningful measures of immunity.

Table 4

Nutritional Supplements for Immune Health in Athletes: Proposed Mechanism of Action and Evidence for Efficacy

Supplement

Proposed Mechanism of Action

Evidence for Efficacy

Vitamin D

An essential fat-soluble vitamin known to influence several aspects of immunity, particularly innate immunity (e.g., expression of antimicrobial proteins). Skin exposure to sunlight accounts for 90% of the source of vitamin D.

Moderate support. Evidence for deficiency in some athletes and soldiers, particularly in the winter (decreased skin sunlight exposure). Deficiency has been associated with increased URS. Recommend 1,000 IU/day D3 autumn–spring to maintain sufficiency. Further support required (He et al., 2016).

Probiotics

Probiotics are live microorganisms which, when administered orally for several weeks, can increase the numbers of beneficial bacteria in the gut. This has been associated with a range of potential benefits to gut health, as well as modulation of immune function.

Low-moderate support. Human studies show some reduction in URS during short periods of intensified training and mild stimulation of mitochondrial biogenesis and endurance performance, albeit in small numbers of untrained subjects. Limited influence on markers of immunity. Putative anti-viral effect for Quercetin. Further support required (Gleeson, 2016; Nieman et al., 2007).

Zinc

An essential mineral that is claimed to reduce incidence and duration of colds. Zinc is required for DNA synthesis and as an enzyme cofactor for immune cells. Zinc deficiency results in impaired immunity (e.g., lymphoid atrophy), and zinc deficiency is not uncommon in athletes.

No support for preventing URS. High doses of zinc can decrease immune function and should be avoided. Moderate support for treating URS. Cochrane review shows benefit of zinc acetate lozenges (75 mg) to decrease duration of URS; however, zinc must be taken <24 hr after onset of URS for duration of cold only. Side effects include bad taste and nausea (Singh & Das, 2013).

Glutamine

Nonessential amino acid that is an important energy substrate for immune cells, particularly lymphocytes. Circulating glutamine is lowered after prolonged exercise and very heavy training.

Found in fish oil. May influence immune function by acting as a fuel, in their role as membrane constituents or by regulating eicosanoid formation (e.g., prostaglandin). Prostaglandin is immunosuppressive. Claimed to exert anti-inflammatory effects postexercise.

Limited support for blunting inflammation and functional changes after muscle-damaging eccentric exercise in humans and no evidence of reducing URS in athletes (Jakeman et al., 2017; Mickleborough, 2013).

No support. Immune-enhancing effects in the frail elderly but no benefit in young, healthy humans. One study actually showed that vitamin E supplementation increased URS in those under heavy exertion. High doses may be pro-oxidative (Hemila et al., 2003; Meydani et al., 2004).

β-glucans

Polysaccharides derived from the cell walls of yeast, fungi, algae, and oats that stimulate innate immunity.

Supplements that assist an athlete to train harder, recover more quickly, and prevent injury or accelerate return to play when injury does occur can obviously enhance the athlete’s preparation and, indirectly, their competition outcomes. Many products claim to provide benefits of this nature. Table 5 summarizes the evidence for some of the most popular compounds. Finally, the manipulation of body composition, including gaining lean (muscle) mass and reducing body fat levels, can contribute to performance in many events. This explains the large number of “weight gainers” and “fat burners” in the general and sports supplement market, though many of these are prohibited in sport. Protein is considered to be the premier ingredient in weight-gain-promoting supplements and evidence-based reviews conclude that protein is effective at promoting lean mass gain when combined with resistive exercise (Hector & Philips, 2018). Evidence of efficacy for “fat burning” supplements is far from conclusive, however, and there is a complete absence of evidence for the effectiveness of the vast majority of supplements marketed in this category. Table 6 summarizes the evidence for some of the most common ingredients or products of this type (Hector & Philips, 2018).

Many studies demonstrate improved training adaptations, such as increased lean mass or strength, indicating an enhanced adaptive response to exercise (Branch, 2003; Heaton et al., 2017; Rawson & Volek, 2003). Reduced symptoms of, or enhanced recovery from, muscle-damaging exercise (e.g., DOMS) have been reported in some, but not all studies (reviewed in (Rawson et al., 2017). Enhanced recovery from disuse or immobilization/extreme inactivity has been reported in some, but not all studies (reviewed in Heaton et al., 2017). Improved cognitive processing is reported in most studies, especially when volunteers were fatigued by sleep deprivation or mental/physical tasks (reviewed in Gualano et al., 2012; 2016; Rae & Broer, 2015; Rawson & Venezia, 2011). The effects in athletes have not been well characterized, and only one group attempted to translate these effects into to athletic performance, albeit with a positive result. (Cook et al., 2011). Decreased damage and enhanced recovery from mTBI is supported by open label trials in children (Sakellaris et al., 2006, 2008) and using animal models (Sullivan et al., 2000). These data are not conclusive and more research is warranted. However, athletes at risk for concussion, who already ingest creatine supplements for performance or muscular benefits, may receive important brain benefits as well. A small increase in body mass is common with supplementation. This may be relevant for sports with weight classes/restrictions or where increased body mass may decrease performance.

Beneficial effects of HMB on strength and fat free mass are small, while the effects on muscle damage are unclear (Rowlands & Thomson, 2009). Recent reports of “steroid-like” gains in strength, power, and fat free mass, and reductions in muscle damage from HMB-free acid (HMB-FA) supplementation (Lowery et al., 2016; Wilson et al., 2013, 2014) have not been reproduced and seem unlikely (Phillips et al., 2017). Potential use for HMB during extreme inactivity/disuse or recovery from injury, but these effects have only been described in older adults following 10 days of bed rest (Deutz et al., 2013). Benefits of HMB supplementation could most likely be obtained from normal dietary protein or whole protein supplements (Wilkinson et al., 2013), so HMB supplements may not be more effective than adhering to the current protein intake recommendations

Improved cognitive processing following omega 3-fatty acid supplementation shown in healthy older adults those with mild or severe cognitive impairment (reviewed in Barrett et al., 2014). It is not known if these benefits would occur in young, healthy athletes, or how this would translate to athletic performance. Animal data show that the structural damage and cognitive decline associated with mTBI are reduced/attenuated with omega-3 fatty acid supplementation when ingested either before or after the injury (reviewed in Barrett et al., 2014; Erdman et al., 2011; Tipton, 2015). Two case studies support these findings (Lewis et al., 2013; Roberts et al., 2008) and large, double-blind, placebo-controlled trials are currently under way (clinicaltrials.gov NCT101903525, NCT01814527). In muscle, omega-3 fatty acid supplementation can increase muscle protein synthesis (Smith et al., 2011a, 2011b), but this may not occur when protein is ingested after exercise in recommended amounts (Smith et al., 2011a, 2011b). Anti-inflammatory effects of omega-3 fatty acid intake may reduce muscle damage or enhance recovery from intense, eccentric exercise (e.g., decrease DOMS), but this is not a consistent finding (Gray et al., 2014; Jouris et al., 2011). No indication that decreased omega 3-fatty acids in the body impair performance, and high-dose supplements can cause some adverse effects (reviewed in (Erdman et al., 2011; Mickleborough, 2013), so the best recommendation may be to include rich sources of omega-3 fatty acids, such as fatty fish, in the diet instead of supplements. Low risk but unclear if supplementation should be pursued by athletes, in lieu of including fatty fish in the diet as a source of omega-3 fatty acids. Fish oil or omega-3 fatty acid supplement consumption could include heavy metal contaminants, or cause bleeding, digestive problems, and/ or increased LDL.

Vitamin D: An essential fat-soluble vitamin. Skin exposure to sunlight normally accounts for 90% of the source of vitamin D.

Anti-inflammatory supplements: Curcumin (a constituent of the spice turmeric) is often ingested for anti-inflammatory effects at a dose of about 5 g/day. Tart cherry juice at a dose of about 250–350 mL (30 mL if concentrate) twice daily for 4 to 5 day before an athletic event or for 2 to 3 days afterwards to promote recovery.

ProteinUsually comprised of isolated proteins from various sources (whey and soy most common)Recommended daily dose: 1.6 g protein/kg/day optimal (up to 2.2 g/kg/day with no adverse effects)Recommended per-meal doses: 0.3–0.5 g protein/kg (3–4 times per day and in close temporal proximity to exercise, with postexercise being consistently shown to be effective)

Enhances lean mass gains when ingested during programs of resistance training due to increased provision of building blocks (amino acids) and leucine as a trigger for a rise in muscle protein synthesis and suppression of muscle protein breakdown

Adverse Effects

Adverse effects from the use of supplements may arise from a number of factors, including the safety and composition of the product per se and inappropriate patterns of use by athletes. Poor practices by athletes include the indiscriminate mixing and matching of many products without regard to total doses of some ingredients or problematic interactions between ingredients. Even commonly-used products may have negative side effects, especially when used outside the optimal protocol. For example, iron supplementation in those with already adequate iron stores can result in symptoms that may begin with vomiting, diarrhea, and abdominal pain, and develop to haemochromatosis and liver failure (Mettler & Zimmermann, 2010). Bicarbonate may cause gastrointestinal distress when ingested in amounts sufficient to enhance performance; this can impair rather than improve performance and may counteract the benefits of other supplements taken at the same time (Carr et al., 2011a). The “more is better” philosophy, when applied to caffeine, may result in side effects, including nausea, anxiety, accelerated heart rate, and insomnia, which outweigh the performance benefits (Peeling et al., 2018). Unwanted outcomes become more common with caffeine doses ≥9 mg/kg body mass, but maximal benefits are usually achieved with intakes of 3–6 mg/kg (Burke, 2008). The possibility of more serious outcomes is illustrated by adverse, and potentially fatal, responses in two separate incidents in which very large doses (up to 30 grams) of caffeine were administered to healthy volunteers participating in laboratory studies (Bodkin, 2017). These incidents were due to errors in the dose calculation—if this can happen in a university research environment with supposed oversight by experienced staff, the potential clearly exists for similar errors by athletes and coaches.

Athletes and members of their support team should be aware of the regulations that govern the manufacture and marketing of supplements. According to the Dietary Supplements Health and Education Act 1994 (DSHEA) passed by US Congress, nutritional supplements sold in the United States that do not claim to diagnose, prevent, or cure disease are not subject to regulation by the Food and Drug Administration (FDA). Similar regulations apply in most other countries, where supplements are regulated in the same way as food ingredients and are therefore not subject to the stringent regulations that are applied to the pharmaceutical industry. This means that there is no requirement to prove claimed benefits, no requirement to show safety with acute or chronic administration, no quality assurance of content, and no liberal labeling requirements. It is well recognized that there are problems with some of the dietary supplements on sale, but the options open to those responsible for food safety are limited by the legislation that applies. The FDA regularly uses its powers to recall products in breach of the regulations, though they fully admit that their resources are insufficient for comprehensive monitoring, and recalls generally occur only after many people are harmed (https://www.fda.gov/food/recallsoutbreaksemergencies/recalls/default.htm). The FDA have recently recalled supplement products containing excessive doses of vitamins A, D, B6, and selenium because of potentially toxic levels of these components. Examples of product complaints have included the presence of impurities, including lead, broken glass, and metal fragments, because of the failure of the producers to observe good manufacturing practice. The risk of gastrointestinal upset because of poor hygiene during the production and storage of products is also of concern. Although this may seem a minor inconvenience, and of similarity to food safety issues, the coincidence of problems around a crucial training period or competitive event may significantly interfere with an athlete’s performance goals. It should be noted, though, that all of these problems are also regularly reported in normal foods.

Some supplements may actually cause harm to health, but these can be difficult to identify, and products are usually withdrawn only after a significant number of adverse events have occurred. For example, a range of products containing hydroxycitric acid were withdrawn from sale, but only after they were linked with the death of one consumer and with a substantial number of other cases of liver toxicity, cardiovascular problems, and seizures (https://www.fda.gov/NewsEvents/PublicHealthFocus/ucm155817.htm). The extent of the problem is illustrated by the fact that, in the United States in 2015, approximately 23,000 emergency department visits annually are reported to be associated with dietary supplement use (Geller et al., 2015). This figure can be viewed as substantial, or it can be seen as small compared to the total number of adverse responses associated with the use of medications (Maughan et al., 2018). However, minor problems that do not require acute medical aid may still be sufficient to interrupt training or prevent participation, so this statistic probably underestimates the risk for athletes.

The biggest concern for athletes who compete under an anti-doping code (usually the World Anti-Doping Code, as published by the World Anti-Doping Agency [WADA]) is that supplements can contain prohibited substances that result in an anti-doping rule violation (ADRV). Athletes—and their support teams—may be at risk for an ADRV if there is evidence that they have used or attempted to use products containing ingredients on the Prohibited List (www.wada.ama.org). A common problem is the recording of an adverse analytical finding (AAF) of a prohibited substance in a urine sample (“positive drug test”) as a result of supplement use (Maughan, 2005). Millions of athletes may be subject to anti-doping testing, although these are mostly professional-, national-, or international-level athletes. For these athletes in particular, even if the ingestion of the prohibited substance was unintentional, the rules of strict liability within the World Anti-Doping Code mean that an AAF will be recorded, and may mean the loss of medals won or records set, as well as financial sanctions and/or temporary or permanent suspension from competition. It also damages the athlete’s reputation and may lead to loss of employment and income through failed sponsorship opportunities. Where there has been deliberate cheating or benefit accrued from the use of a prohibited substance, these penalties seem entirely appropriate, but it is undoubtedly true that some ADRVs can be attributed to the innocent ingestion of prohibited substances in dietary supplements, with catastrophic results for the athlete.

One cause of an AAF arising from supplement use relates to an athlete’s failure to read product labels to recognize the presence of prohibited substances. Many athletes consider supplements to be “natural” or “regulated” and therefore safe. Other athletes are confused by the number of chemical names for some prohibited substances and thus fail to recognize them on the product label. However, the most worrying cause of an inadvertent AAF is the use of supplements that contain prohibited substances as an undeclared ingredient or contaminant. Since the publication of the seminal study on the presence of undeclared prohibited substances in supplements (Geyer et al., 2004), there have been numerous reports of supplement contamination (Maughan, 2005). Recent reviews suggest that this problem remains (LGC, 2017; Martinez-Sanz et al., 2017). It is difficult to gain a perspective of the true prevalence of supplement contamination. Although the original study reported that ∼15% of more than 600 products acquired from around the world contained undeclared prohormones (Geyer et al., 2004), this and other investigations rarely include a truly random sample of the supplements and sports foods used by athletes. Some individual products or categories of products can be considered inherently more at risk of contamination due to the country of origin, the manufacturer, the type of product, and the range of declared ingredients (https://www.usada.org/substances/supplement-411/). Nevertheless, it should also be recognized that common supplements, including vitamin C, multivitamins, and minerals, have also been found, albeit rarely, to contain prohibited substances (Geyer et al., 2008). The range of prohibited substances found as undeclared ingredients in supplements now includes products from many sections of the WADA’s List of Prohibited Substances and Methods, including stimulants, anabolic agents, selective androgen receptor modulators, diuretics, anorectics, and β2 agonists (Martinez-Sanz et al., 2017).

In some cases, the amount of the prohibited substance in a supplement may be high, even higher than the normal therapeutic dose. For example, Geyer et al. (2002) reported the analysis of metandienone (commonly known as methandrostenolone or Dianabol) in high amounts in a “body building” supplement from England. The recommended amount of the supplement would have supplied a dose of 10–43 mg; in comparison, the typical therapeutic dose of this drug was 2.5–5 mg/day (Goodman & Gilman, 1975), though its medical use has been discontinued in most countries for many years. This amount would certainly have a potent anabolic effect, but would likely produce serious side effects, including psychiatric and behavioral effects and significant damage to a range of body systems including the liver (Solimini et al., 2017). Unlike many of the earlier cases involving steroids related to nandrolone and testosterone, this is not a trivial level of contamination and raises the possibility of deliberate adulteration of the product with the intention of producing a measurable effect on muscle strength and muscle mass. Most reports of adverse health outcomes resulting from supplement use have focused on liver problems of varying degrees of severity, but other organs are also affected. One epidemiological case-control study (Li et al., 2015) examined the association between use of muscle-building supplements and testicular germ cell cancer (TGCC) risk, with 356 TGCC cases and 513 controls from the Eastern United States. The odds ratio (OR) for the use of muscle-building supplements in relation to risk of TGCC was elevated (OR = 1.65, 95% confidence interval [CI]: 1.11–2.46), with significantly stronger associations for early users and longer periods of use.

Ironically, supplements that are contaminated with extremely small amounts of prohibited substances (too low to have any physiological effect) may still cause a positive doping outcome. For instance, ingestion of 19-norandrostenedione, a precursor of nandrolone, will result in the appearance in the urine of 19-norandrosterone, the diagnostic metabolite for nandrolone. If the urinary concentration of 19-norandrosterone exceeds 2 ng/mL, an AAF is recorded (Baume et al., 2004). The addition of as little as 2.5 µg of 19-norandrostenedione to a supplement can result in a urinary concentration of 19-norandrosterone that exceeds this threshold (Watson et al., 2009). These amounts are close to the limits of detection of the analytical methods currently applied to the analysis of dietary supplements, and are far below the levels of contamination deemed acceptable from a health and safety perspective.

Various efforts are being made to address the problems, including the use of third-party auditing activities to identify products that athletes may consider to be at “low risk” of containing prohibited substances. There can be no absolute guarantee that any product is entirely safe, but these schemes do help the athlete to manage the risk. Athletes contemplating the use of dietary supplements should consider very carefully whether the possible benefits outweigh the risks of a doping offense that might end their career.

Practical Implications and Decision Tree

Dietary supplements are an established part of the landscape of modern sport and are likely to remain so. Athletes who take supplements often have no clear understanding of the potential effects of supplements they are using, but supplements should be used only after a careful cost-benefit analysis has been conducted. On one side of the decision tree are the rewards, the most obvious of which are correction of nutrient deficiencies, achievement of nutritional goals, or enhancement of one or another physiological/biochemical function to directly or indirectly improve performance. On the other side lie the costs—the possibility of using an ineffective supplement, the possible risks to health, and the potential for an ADRV. A flow of questions that could be posed in reaching an informed decision is shown in Figures 2 and 3.

In deciding whether to use a supplement, athletes should consider all aspects of their maturation in, and preparation for, their event to ensure that the supplement under consideration provides an advantage that no other strategy can address. Whether the supplement is practical to use should also be assessed: Is the product available, affordable, tolerated, and compatible with the athlete’s other goals? The input of the athlete’s coaching team and medical/science support network is important. Athletes who do not have regular access to such a network should consider decisions around supplement use as an important reason to consult an independent sports nutrition expert as well as a physician. Analysis of the evidence around the effectiveness of supplements and their safety is often difficult. A complete nutritional assessment may provide an appropriate justification for the specific use of nutritional supplements and sports foods. For a small number of sports supplements, there is good evidence of a performance effect or indirect benefit for some athletes in some specific situations with little or no risk of adverse outcomes (Peeling et al., 2018; Rawson et al., 2018). Professional advice is often important in ensuring that the athlete is sufficiently knowledgeable about the appropriate protocol for use of these supplements, but individual athletes may respond very differently to a given supplement, with some exhibiting a markedly beneficial effect while others experience no benefit or even a negative effect on performance. Furthermore, the situation in which the athlete wishes to use the supplement may differ in important ways from its substantiated use. Repeated trials may be necessary to establish whether a true effect, rather than just random variation, is seen in response to use of any novel intervention. Some trial and error may also be involved in fine tuning the supplement protocol to suit the needs of the specific situation of use or the individual athlete.

Evidence to support the effectiveness and safety of many of the supplements targeted at athletes, however, is largely absent. There seems to be little incentive for those selling supplements to invest the substantial sums needed to undertake detailed scientific evaluation of their products. Even where some evidence does exist, it may not be relevant to the high-performance athletes because of limitations in the study design (such as the specificity of the exercise tests), the study population, or the context of use. Failure to verify the composition of the supplements used may also give misleading results. It seems sensible to exercise caution when using supplements, as any compound that has the potential to enhance health or exercise performance by altering physiological function must also have the potential for adverse effects in some individuals. Athletes should see good evidence of a performance or other benefit, and should be confident that it will not be harmful to health, before accepting the financial cost and the health or performance risks associated with any supplement. Finally, the athlete should be sure, if supplements or sports foods are to be used, that they have undertaken due diligence to source products that are at low risk of containing prohibited substances.

Conclusion

Dietary supplements can play a small role in an athlete’s sports nutrition plan, with products that include essential micronutrients, sports foods, performance supplements, and health supplements all potentially providing benefits. Some supplements, when used appropriately, may help athletes to meet sports nutrition goals, train hard, and stay healthy and injury free. A few supplements can directly enhance competition performance. However, it takes considerable effort and expert knowledge to identify which products are appropriate, how to integrate them into the athlete’s sports nutrition plan, and how to ensure that any benefits outweigh the possible negative side effects, including the potential for an ADRV. A strict risk-benefit analysis involving a decision tree approach to the effectiveness, safety, and risks should identify the small number of products that may benefit the athlete. Such an analysis requires the input of a well-informed sports nutrition professional.

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*Note. This article is co-published with the British Journal of Sports Medicine (April 2018, Vol. 52, Issue 7; doi:10.1136/bjsports-2018-099027). Maughan and Shirreffs are with St Andrews University, St Andrews, UK. Burke is with the Australian Institute of Sport, Canberra, Australia. Burke and van Loon are with the Mary MacKillop Institute for Health Research, Melbourne, Australia. Dvorak is with Schulthess Clinic, Zurich, Switzerland. Larson-Meyer is with the University of Wyoming, Laramie, WY. Peeling is with The University of Western Australia, Crawley, Australia, and with the Western Australian Institute of Sport, Mt Claremont, Australia. Phillips is with McMaster University, Hamilton, Ontario, Canada. Rawson is with Messiah College, Mechanicsburg, PA. Walsh is with Bangor University, Bangor, United Kingdom. Garthe is with the Norwegian Olympic and Paralympic Committee and Confederation of Sport, Oslo, Norway. Geyer is with German Sport University, Cologne, Germany. Meeusen is with Vrije Universiteit Brussel, Brussels, Belgium. van Loon is also with Maastricht University Medical Centre, Maastricht, The Netherlands. Spriet is with the University of Guelph, Guelph, Ontario, Canada. Stuart is with BMJ, London, United Kingdom. Vernec is with the World Anti-Doping Agency, Montreal, Quebec, Canada. Currell is with the English Institute of Sport, Loughborough, United Kingdom. Ali, Budgett, Pitsiladis, Soligard, Erdener, and Engebretsen are with the International Olympic Committee, Lausanne, Switzerland. Ljungqvist is with the The Professor Arne Ljungqvist Anti-Doping Foundation, Stockholm, Sweden. Mountjoy is with the University of Guelph, Guelph, Ontario, Canada.

BodkinH. (2017). Students left fighting for lives after taking enough caffeine for 300 cups of coffee in botched university experiment. The Telegraph. Retrieved from http://www.telegraph.co.uk/news/2017/01/25/university-fined-400k-students-taking-part-caffeine-experiment/

Bodkin, H. (2017). Students left fighting for lives after taking enough caffeine for 300 cups of coffee in botched university experiment. The Telegraph. Retrieved from http://www.telegraph.co.uk/news/2017/01/25/university-fined-400k-students-taking-part-caffeine-experiment/)| false